Dataset Information

Humin oxidation is a Survival Strategy of Organohalide-respiring Bacteria in Oligotrophic Environments

ABSTRACT: This project investigates the survival strategies of organohalide-respiring bacteria in oligotrophic environments, focusing on their mechanisms of energy acquisition through humins oxidation. The research aims to uncover the metabolic adaptability of bacteria in resource-limited settings, providing new insights into microbial survival strategies under extreme conditions. It may also have significant implications for bioremediation and environmental pollution management.

INSTRUMENT(S):

ORGANISM(S): Pseudomonas Aeruginosa Pao579

TISSUE(S): Cell Culture, Electrically Active Cell

DISEASE(S): Acute Leukemia

SUBMITTER: Zimeng Zhang

LAB HEAD: Li Zhiling

PROVIDER: PXD061683 | Pride | 2025-10-13

REPOSITORIES: Pride

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Publications

Humin oxidation drives microbial dehalogenation in oligotrophic environments.

Zhang Zimeng Z Liu Xing X Li Zhiling Z Chen Xueqi X Zu Yunxia Y Ho Shih-Hsin SH Liang Bin B Zhou Shungui S Wang Aijie A

The ISME journal 20250101 1

Energy acquisition presents a fundamental constraint for microbial survival in oligotrophic environments. Although heterotrophic organohalide-respiring bacteria (OHRB) are known to perform reductive dehalogenation in organohalide-contaminated oligotrophic ecosystems, their energy metabolism remains poorly understood. Here, we report that Pseudomonas sp. CP-1, an organohalide-respiring bacterium, can directly oxidize humin from diverse oligotrophic aquifers to drive organohalide respiration. Spec ...[more]

PMID: 40972878

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Project description:The strictly anaerobic bacterium Dehalococcoides mccartyi is obligatory dependent on organohalide respiration for energy conservation and growth. Due to its capability to reductively dehalogenate a multitude of toxic halogenated electron acceptors, it plays an important role in the attenuation of these compounds at respective contaminated sites. Here, D. mccartyi strain CBDB1, specialized on the dehalogenation of chloroaromatic compounds, was grown in a two-liquid phase system with 1,2,3-trichlorobenzene as electron acceptor, acetate plus CO2 as carbon source and hydrogen as electron donor. The proteome and Nε-lysine acetylome were analyzed in the lag, exponential and stationary phases. The high and almost invariable abundance of the membrane-localized organohalide respiration complex consisting of the reductive dehalogenases CbrA and CbdbA80, the uptake hydrogenase HupLS and the organohalide respiration molybdoenzyme OmeAB was shown throughout growth and also after a prolonged stationary phase. Quantification of transcripts of reductive dehalogenase genes revealed their major synthesis starting in the lag phase, which might be a prerequisite for balanced growth in the exponential phase. The analyses of the coverage of functional pathways as well as indicator analysis revealed the growth-phase specificity of the proteome, with regulatory proteins identified as important indicators for the stationary phase. The number of acetylated proteins increased from the lag to the stationary phase. We detected pronounced acetylation of key proteins of the acetate metabolism, i.e. the synthesis of acetyl-CoA and its processing via gluconeogenesis and the incomplete Wood-Ljungdahl pathway, as well as of proteins central for the biosynthesis of amino acids, co-factors and terpenoids. In addition, the partial acetylation of the reductive dehalogenases as well as of TatA, a component of the twin-arginine translocation machinery, suggests that acetylation might be directly involved in the maintenance of the organohalide respiration capacity of D. mccartyi over periods without access to halogenated electron acceptors.

Project description:Desulfitobacterium hafniense was originally isolated for its ability to use organohalogens as terminal electron acceptors in the process of organohalide respiration (OHR). However, in contrast to obligate OHR bacteria, Desulfitobacterium spp. show a highly versatile energy metabolism with the capacity to use many possible electron donors and acceptors and to grow fermentatively also. The sequencing of several Desulfitobacterium genomes displaying numerous and apparently redundant members of redox enzyme families has confirmed their large metabolic potential. Nonetheless, the enzymes responsible for many metabolic traits are not yet identified. In the present work, we conducted an extended proteomic study by comparing the proteomes of D. hafniense strain DCB-2 cultivated in different combinations of electron donors and acceptors, triggering five alternative respiratory metabolisms that include OHR, as well as fermentation. The Tandem Mass Tag labelling proteomic approach allowed us to identify almost 60% of the predicted proteome of strain DCB-2 in all six growth conditions and to quantify the relative abundance of 2796 proteins. This dataset was analysed in order to highlight the proteins that were up-regulated in one or a subset of growth conditions to identify possible key players in the different energy metabolisms. The addition of sodium sulfide as reducing agent in the medium – a very widespread practice in the cultivation of strictly anaerobic bacteria – triggered the expression of the dissimilatory sulfite reduction pathway in relatively less favourable conditions such as fermentative growth on pyruvate, respiration with H2 as electron donor and OHR conditions. The presence of H2, CO2 and acetate in the medium induced several metabolic pathways involved in carbon metabolism including the Wood-Ljungdahl pathway and two pathways related to the fermentation of butyrate that rely on electron-bifurcating enzymes. While the predicted fumarate reductase appears to be constitutively expressed, a new lactate dehydrogenase and lactate transporters were identified. Finally, the OHR metabolism with 3-chloro-4-hydroxyphenylacetate as electron acceptor strongly induced proteins encoded in several reductive dehalogenase gene clusters including four new proteins, the function of which is discussed. Overall, we believe that this extended proteomic database represents a new landmark in understanding the metabolic versatility of Desulfitobacterium spp. and provides a solid basis for addressing present and future research questions.

Project description:BackgroundMassive amounts of sewage sludge are generated during biological sewage treatment and are commonly subjected to anaerobic digestion, land application, and landfill disposal. Concurrently, persistent organic pollutants (POPs) are frequently found in sludge treatment and disposal systems, posing significant risks to both human health and wildlife. Metabolically versatile microorganisms originating from sewage sludge are inevitably introduced to sludge treatment and disposal systems, potentially affecting the fate of POPs. However, there is currently a dearth of comprehensive assessments regarding the capability of sewage sludge microbiota from geographically disparate regions to attenuate POPs and the underpinning microbiomes.ResultsHere we report the global prevalence of organohalide-respiring bacteria (OHRB) known for their capacity to attenuate POPs in sewage sludge, with an occurrence frequency of ~50% in the investigated samples (605 of 1186). Subsequent laboratory tests revealed microbial reductive dechlorination of polychlorinated biphenyls (PCBs), one of the most notorious categories of POPs, in 80 out of 84 sludge microcosms via various pathways. Most chlorines were removed from the para- and meta-positions of PCBs; nevertheless, ortho-dechlorination of PCBs also occurred widely, although to lower extents. Abundances of several well-characterized OHRB genera (Dehalococcoides, Dehalogenimonas, and Dehalobacter) and uncultivated Dehalococcoidia lineages increased during incubation and were positively correlated with PCB dechlorination, suggesting their involvement in dechlorinating PCBs. The previously identified PCB reductive dehalogenase (RDase) genes pcbA4 and pcbA5 tended to coexist in most sludge microcosms, but the low ratios of these RDase genes to OHRB abundance also indicated the existence of currently undescribed RDases in sewage sludge. Microbial community analyses revealed a positive correlation between biodiversity and PCB dechlorination activity although there was an apparent threshold of community co-occurrence network complexity beyond which dechlorination activity decreased.ConclusionsOur findings that sludge microbiota exhibited nearly ubiquitous dechlorination of PCBs indicate widespread and nonnegligible impacts of sludge microbiota on the fate of POPs in sludge treatment and disposal systems. The existence of diverse OHRB also suggests sewage sludge as an alternative source to obtain POP-attenuating consortia and calls for further exploration of OHRB populations in sewage sludge. Video Abstract.

Project description:Dehalococcoides mccartyi (Dhc) and Dehalogenimonas spp. (Dhgm) are members of the class Dehalococcoidia, phylum Chloroflexi, characterized by streamlined genomes and a strict requirement for organohalogens as electron acceptors. Here, we used cryo-electron tomography to reveal morphological and ultrastructural features of Dhc strain BAV1 and "Candidatus Dehalogenimonas etheniformans" strain GP cells at unprecedented resolution. Dhc cells were irregularly shaped discs (890 ± 110 nm long, 630 ± 110 nm wide, and 130 ± 15 nm thick) with curved and straight sides that intersected at acute angles, whereas Dhgm cells appeared as slightly flattened cocci (760 ± 85 nm). The cell envelopes were composed of a cytoplasmic membrane (CM), a paracrystalline surface layer (S-layer) with hexagonal symmetry and ∼22-nm spacing between repeating units, and a layer of unknown composition separating the CM and the S-layer. Cell surface appendages were only detected in Dhc cells, whereas both cell types had bundled cytoskeletal filaments. Repetitive globular structures, ∼5 nm in diameter and ∼9 nm apart, were observed associated with the outer leaflet of the CM. We hypothesized that those represent organohalide respiration (OHR) complexes and estimated ∼30,000 copies per cell. In Dhgm cultures, extracellular lipid vesicles (20 to 110 nm in diameter) decorated with putative OHR complexes but lacking an S-layer were observed. The new findings expand our understanding of the unique cellular ultrastructure and biology of organohalide-respiring Dehalococcoidia. IMPORTANCE Dehalococcoidia respire organohalogen compounds and play relevant roles in bioremediation of groundwater, sediments, and soils impacted with toxic chlorinated pollutants. Using advanced imaging tools, we have obtained three-dimensional images at macromolecular resolution of whole Dehalococcoidia cells, revealing their unique structural components. Our data detail the overall cellular shape, cell envelope architecture, cytoskeletal filaments, the likely localization of enzymatic complexes involved in reductive dehalogenation, and the structure of extracellular vesicles. The new findings expand our understanding of the cell structure-function relationship in Dehalococcoidia with implications for Dehalococcoidia biology and bioremediation.

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